From 1961-66, Halperin taught at Harvard University's Center for International Affairs. During this Cold War period, he advocated for U.S. nuclear disarmament even if the Soviet Union did not likewise disarm. In any mutual arms-reduction treaty with the Soviets, wrote Halperin in his 1961 treatiseA Proposal for a Ban on the Use of Nuclear Weapons, “inspection was not absolutely necessary.… The United States might, in fact, want to invite the Soviets to design the inspection procedures if they seem interested in them.”

In testimony which he gave before the Senate Foreign Relations Committee in 1966, Halperin stated that the U.S. should diplomatically recognize the Communist People's Republic of China and advocate for its admission to the United Nations.

From 1966-69 Halperin served as deputy assistant secretary of defense under President Lyndon Johnson, whose administration put Halperin in charge of compiling a classified history of U.S. military involvement in Vietnam. As David Horowitz and Richard Poe report: “This secret history later emerged [in June 1971] into public view as the so-called 'Pentagon Papers.' Halperin and his deputy Leslie Gelb assigned much of the writing to leftwing opponents of the war, such as Daniel Ellsberg … With Halperin's tacit encouragement – and perhaps active collusion – Ellsberg stole the secret history and released it to The New York Times.… Not surprisingly, 'The Pentagon Papers' echoed Halperin's longstanding position that the Vietnam War was unwinnable, and ridiculed Presidents Kennedy and Johnson for stubbornly refusing to heed those of their advisers who shared this opinion.” In a 1973 federal trial in which Ellsberg was charged with violations of the Espionage Act, Halperin testified on behalf of the defendant.

When Richard Nixon began his first term as U.S. president in January 1969, Halperin was named as a senior assistant to then-National Security Advisor Henry Kissinger. Halperin resigned that post in 1970, however, as a protest against Nixon's decision to move American forces into Cambodia and to intensify the bombing of North Vietnam.

In 1970 as well, Halperin became a Senior Fellow at the Brookings Institution. Meanwhile, he was feted and embraced by numerous leftist organizations that promoted similar views, such as the Carnegie Endowment for International Peace and the Council on Foreign Relations.

During that same time period, Halperin served on the executive council and newsletter committee of the ACLU's Committee for Public Justice, a Communist-affiliated entity which was created in 1970 to discredit the FBI, CIA, and Justice Department as agents of political repression.

In his 1971 book Defense Strategies for the Seventies, Halperin wrote: “The Soviet Union apparently never contemplated the overt use of military force against Western Europe. The Soviet posture … has been, and continues to be, a defensive and deterrent one … against a Western attack.”

In the mid-1970s Halperin befriended Philip Agee, a former CIA agent-turned-Cuban intelligence informant who, in a 1975 book, publicly disclosed the names of more than 700 CIA officers, agents, and cooperators worldwide. At least one of the CIA agents, Athens station chief Richard Welch, was murdered shortly after the publication of Agee's book. In an extremely favorable review of the book, Halperin wrote that the most prudent course of action for the U.S. would be “to dissolve the CIA covert career service and to bar the CIA from at least developing and allied nations.” Moreover, Halperin flew to Europe in 1977 in an unsuccessful attempt to help Agee find safe haven after Great Britain had expelled him. And in the U.S., Halperin testified repeatedly against legislation proposing to punish those who revealed -- as Agee had done -- the identities of U.S. undercover agents.

In testimony he gave before the Church Committee on December 5, 1975, Halperin said: “I believe that the United States should no longer maintain a career service for the purpose of conducting covert operations and covert intelligence collection by human means. I believe also that the United States should eschew, as a matter of national policy, the conduct of covert operations.”

That same year, Halperin became the chief editorial writer for First Principles, a monthly CNSS publication designed to advance the campaign against U.S. intelligence collection.

In the mid-1970s as well, Halperin served as director of the Project on National Security and Civil Liberties, the litigating arm of the ACLU's campaign to degrade and destroy America's intelligence capabilities.

In 1976 Halperin co-authored the book The Lawless State: The Crimes of the U.S. Intelligence Agencies. That same year, he accusedthe FBI of “murdering” Black Pantherleader Fred Hampton.

In 1977 Halperin became chairperson of the Campaign to Stop Government Spying (CSGS), which was launched in 1977 by Robert Borosage with the support of the IPS, the ACLU, the CNSS, and the NLG. CSGS also had close ties to the Socialist Workers Party and Philip Agee's Organizing Committee for a Fifth Estate, and it later changed its name to the Campaign for Political Rights.

Under the auspices of the ACLU's Washington, DC office, Halperin in 1979 defended the right of The Progressivemagazine to publish secret details it had obtained regarding how to build a hydrogen bomb.

In the June 9, 1979 issue of The Nationmagazine, Halperin wrote the following with regard to the Soviet-Cuban military intervention in Angola: “Every action which the Soviet Union and Cuba have taken in Africa has been consistent with the principles of international law.”

In Target America – James L. Tyson's 1981 exposé of the Soviet Union's massive “propaganda campaign designed to weaken and demoralize America from the inside”[1]– the author stated: “Halperin has emerged as probably the leading 'expert' on intelligence matters among the Far Left Lobby groups. He and his organizations have had a constant record of advocating the weakening of U.S. intelligence capabilities. His organizations are also notable for ignoring the activities of the KGB or any other foreign intelligence organization. His criticism of American intelligence misdeeds would give the impression that our agencies have been committing these crimes simply for their own villainous reasons in a world where the U.S. faces no external enemies whatever. A balance sheet analysis of Halperin's writings and testimonies ... gives Halperin a score of 100% on the side of output favorable to the Communist line and 0% on any output opposed to the Communist line.”[2]

In 1984 Halperin became thedirector of the ACLU's Washington, DC office.

According to a May 2000 reportin World Net Daily: “[A] well-respected former State official … who worked in intelligence during the height of the Cold War” described Halperin as “a person we knew to be pro-Soviet,” “not a person to be trusted,” and a man who was “known on embassy [briefing] cards as a Soviet or communist agent.”

During his tenure as CNSS director, Halperin filed numerous Freedom Of Information Act (FOIA) requests in an effort to procure secret data from the files of U.S. intelligence and security agencies. On some occasions, he followed up those FOIA requests with lawsuits.

Halperin retained his directorships with both the CNSS and the ACLU until the end of October 1992, at which time he became a senior associate at the Carnegie Endowment for International Peace and a professor at George Washington University.

In February 1993, newly elected President Bill Clintonannounced his appointmentof Halperin to the new position of Assistant Secretary of Defense for Democracy and Peacekeeping. Halperin withdrew his name from consideration in January 1994, however, when his nomination was stalled by both Republican and Democrat U.S. senators who refused to consent to a nominee with so radical a history. Clinton thereafter appointed Halperin to several positions that required no Senate confirmation: “Consultant to the Secretary of Defense and the Under Secretary of Defense for Policy” (1993), “Special Assistant to the President” and “Senior Director for Democracy” at the National Security Council (1994-96), and “Director of the Policy Planning Staff” at the Department of State (1998–2001).

During Halperin'stenure at the U.S. State Department, 15 government computers containing highly classified intelligence information mysteriously disappeared; one of them had been checked out to Halperin's office. A number of people were punished for this serious security breach, but Halperin was not.

In February 2002, Halperin became director of the Open SocietyPolicy Center and worked closely with its creator, George Soros. According to a March 1, 2004 report by Robert Dreyfuss in The Nation, Halperin and Soros together hand-picked former Clinton White House chief-of-staff John Podesta to serve as president of the Center for American Progress(CAP). Halperin himself became CAP's senior vice president, and his son David joined the organization as a special advisor on campus outreach. Another of Morton Halperin's sons, Mark Halperin, has been an influential media figure with such outlets as ABC, NBC, MSNBC, and Bloomberg News.